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Decreased motility of flagellated microalgae long-term acclimated to CO2-induced acidified waters

Nature Climate Change volume 10, pages 561–567 (2020)Cite this article

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Abstract

Motility plays a critical role in algal survival and reproduction, with implications for aquatic ecosystem stability. However, the effect of elevated CO2 on marine, brackish and freshwater algal motility is unclear. Here we show, using laboratory microscale and field mesoscale experiments, that three typical phytoplankton species had decreased motility with increased CO2. Polar marine Microglena sp., euryhaline Dunaliella salina and freshwater Chlamydomonas reinhardtii were grown under different CO2 concentrations for 5 years. Long-term acclimated Microglena sp. showed substantially decreased photo-responses in all treatments, with a photophobic reaction affecting intracellular calcium concentration. Genes regulating flagellar movement were significantly downregulated (P < 0.05), alongside a significant increase in gene expression for flagellar shedding (P < 0.05). D. salina and C. reinhardtii showed similar results, suggesting that motility changes are common across flagellated species. As the flagella structure and bending mechanism are conserved from unicellular organisms to vertebrates, these results suggest that increasing surface water CO2 concentrations may affect flagellated cells from algae to fish.

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Fig. 1: Average velocity of Microglena sp. induced by artificial light and sunlight in the field.
Fig. 2: CO2 concentration effects on proportion of Microglena sp. showing deflagellation and restoration of motility.
Fig. 3: Changes in the expression of motility-related genes.
Fig. 4: Distribution of Microglena sp. and light intensity under melting ice.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request. Source Data for Figs. 1–4 and Extended Data Figs. 1–4 are provided with the paper.

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Acknowledgements

This work was supported by the national key research and development programme of China (grant no. 2018YFD0900703); Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (grant no. 2018SDKJ0406-3); Major Scientific and Technological Innovation Project of Shandong Provincial Key Research and Development Program (grant no. 2019JZZY020706); Central Public-interest Scientific Institution Basal Research Fund, CAFS (grant no. 2020TD27); China Agriculture Research System (grant no. CARS-50); Financial Fund of the Ministry of Agriculture and Rural Affairs, P.R. China (grant no. NFZX2018); Taishan Scholars Funding and Talent Projects of Distinguished Scientific Scholars in Agriculture.

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Authors and Affiliations

  1. Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, China

    Yitao Wang, Xiao Fan, Dong Xu, Xiaowen Zhang, Wentao Han & Naihao Ye

  2. Function Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China

    Yitao Wang & Naihao Ye

  3. State Key Laboratory of Marine Environmental Science & College of Ocean and Earth Sciences, Xiamen University, Xiamen, China

    Guang Gao & John Beardall

  4. School of Biological Sciences, Monash University, Clayton, Victoria, Australia

    John Beardall

  5. Shimoda Marine Research Center, University of Tsukuba, Shizuoka, Japan

    Kazuo Inaba & Jason M. Hall-Spencer

  6. School of Biological and Marine Sciences, University of Plymouth, Plymouth, UK

    Jason M. Hall-Spencer

  7. Institute of Antarctic and Southern Ocean Studies, University of Tasmania, Tasmania, Australia

    Andrew McMinn

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Contributions

N.H.Y. designed the project. Y.T.W., D.X., X.W.Z. and W.T.H. performed the research. F.X., N.H.Y. and Y.T.W. analysed the data. Y.T.W., N.H.Y., G. G. and F.X. wrote the first draft. All authors contributed to interpreting the data and writing the manuscript.

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Correspondence to Naihao Ye.

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The authors declare no competing interests.

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Peer review information Nature Climate Change thanks Jolanda Verspagen and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Average velocity of C. reinhardtii and D. salina.

a, C. reinhardtii positive phototaxis induced by white light in the vertical direction. b, C. reinhardtii negative phototaxis induced by white light in the vertical direction. c, D. salina positive phototaxis induced by white light in the vertical direction. d, D. salina negative phototaxis induced by white light in the vertical direction. e, C. reinhardtii positive phototaxis induced by white light in the horizontal direction. f, C. reinhardtii negative phototaxis induced by white light in the horizontal direction. g, D. salina positive phototaxis induced by white light in the horizontal direction. h, D. salina negative phototaxis induced by white light in the horizontal direction. Mean ± SD values per experimental assay are given (n = 3).

Source data

Extended Data Fig. 2 Instantaneous velocity of Microglena sp.

a, Positive phototaxis induced by white light in the vertical direction. b, Negative phototaxis induced by white light in the vertical direction. c, Positive phototaxis induced by white light in the horizontal direction. d, Negative phototaxis induced by white light in the horizontal direction. The colour scale indicates the density of the cell distribution under various velocities. A total of 300 data points was collected for each experimental treatment. The five dotted lines correspond to 0%, 25%, 50%, 75%, 100%, respectively. Each dotted line represents the cumulative ratio, the number of cells below the dotted line as a percentage of the total number of cells. The solid line represents the average velocity and letters indicate significant differences between CO2 treatments (P < 0.05). Different letters in superscript indicate significant differences (P < 0.05) among treatments (Kruskal Wallis test followed by Dunn’s post-hoc test).

Source data

Extended Data Fig. 3 Instantaneous velocity of C. reinhardtii and D. salina in the vertical direction.

a, C. reinhardtii positive phototaxis induced by white light. b, C. reinhardtii negative phototaxis induced by white light. c, D. salina positive phototaxis induced by white light. d, D. salina negative phototaxis induced by white light. The colour scale indicates the density of the cell distribution under various velocities. A total of 300 data points was collected for each experimental treatment. The five dotted lines correspond to 0%, 25%, 50%, 75%, 100%, respectively. Each dotted line represents the cumulative ratio, the number of cells below the dotted line as a percentage of the total number of cells. The solid line represents the average velocity and letters indicate significant differences between CO2 treatments (P < 0.05). Different letters in superscript indicate significant differences (P < 0.05) among treatments (Kruskal Wallis test followed by Dunn’s post-hoc test).

Source data

Extended Data Fig. 4 Instantaneous velocity of C. reinhardtii and D. salina in the horizontal direction.

a, C. reinhardtii positive phototaxis induced by white light. b, C. reinhardtii negative phototaxis induced by white light. c, D. salina positive phototaxis induced by white light. d, D. salina negative phototaxis induced by white light. The colour scale indicates the density of the cell distribution under various velocities. A total of 300 data points was collected for each experimental treatment. The five dotted lines correspond to 0%, 25%, 50%, 75%, 100%, respectively. Each dotted line represents the cumulative ratio, the number of cells below the dotted line as a percentage of the total number of cells. The solid line represents the average velocity and letters indicate significant differences between CO2 treatments (P < 0.05). Different letters in superscript indicate significant differences (P < 0.05) among treatments (Kruskal Wallis test followed by Dunn’s post-hoc test).

Source data

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Wang, Y., Fan, X., Gao, G. et al. Decreased motility of flagellated microalgae long-term acclimated to CO2-induced acidified waters. Nat. Clim. Chang. 10, 561–567 (2020). https://doi.org/10.1038/s41558-020-0776-2

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